By influencing nutrient mineralization in the soil, decomposers may affect the performance of plants and their associated herbivores. The strength of above-belowground linkages may therefore depend on the availability of nutrients in ecosystems. We investigated the dependency of decomposer- and leaf-herbivore-mediated changes in plant performance on soil nutrient availability in microcosm systems. In separate treatments, Poa annua was used as host plant for the herbivore and was grown in combination with different herb species: Plantago lanceolata, Trifolium repens, and Sanguisorba minor. At three different levels of nutrient availability, the impact of Collembola (Folsomia candida) and aphids (Rhopalosiphum padi), as well as their interacting effects on plant performance, were investigated. We further assessed the effects of Collembola on the performance of aphids and vice versa, as well as the effects on element contents in P. annua and soil nutrients.

Collembola increased total aboveground biomass and biomass of single plant species (except T. repens) only at low and moderate nutrient availability, whereas the negative effects of aphids on P. annua and total aboveground biomass were highest at high nutrient availability. Collembola decreased relative root allocation. The negative effect of aphids on plant biomass was more pronounced in the presence of Collembola. Nitrogen concentration in shoots of P. annua was increased by Collembola. Aphids decreased the nitrogen concentration in grass shoots only when Collembola were present. These interacting effects can be related to indirect effects of decomposers on herbivore performance. At low and moderate nutrient availability, aphid numbers strongly increased due to decomposers, whereas at high nutrient availability this effect was much weaker. In turn, aphid herbivory increased the number of Collembola only at high nutrient availability.

We conclude that the role of both below- and aboveground food webs for the dynamics of vegetation depend on each other and the availability of nutrients in ecosystems. This suggests that nutrient enrichment of ecosystems may have important consequences for above belowground linkages and their effects on natural communities.